IntroductionTop
The Maghrebian territory, located in the western and more arid part of the Mediterranean Basin, is recognized as a biodiversity hotspot (Myers et al., 2000). Within the Maghreb, Morocco is particularly interesting for faunistic, ecological and biogeographical studies thanks to its geographical position; it represents a contact area between several regions, such as southern Europe and Africa. Its importance is associated with its role as a compulsory passage area for much of the fauna between the Palaearctic and Afrotropical regions.
The fauna of Morocco is characterized by a high rate of endemism (Taybi et al., 2019; Mabrouki et al., 2020a). The country has multiple geographical barriers, such as the Moulouya River Basin, the Sahara, the Rif Mountains and the Atlas Mountains. The latter divide the northern part of the country into two bioclimatic regions, which in turn are associated with high levels of endemism (Mabrouki et al., 2019a). This high endemicity makes communities vulnerable to the arrival of new invasive species lacking a shared evolutionary history (Ellender et al., 2015). Freshwater biodiversity and habitats are increasingly being affected by human activities worldwide, and freshwater ecosystems may well be the most endangered ecosystems in the world (Stiassny, 1999), particularly by biological invasions (Dukes & Mooney, 1999).
Invasive species are a major threat to global biodiversity, causing the decline and extinction of native aquatic species throughout the world (Strauss et al., 2006). Growth in international trade and concurrent increases in transport capacity have accelerated the rate of introduction of alien species worldwide, with aquatic ecosystems and their native communities being particularly susceptible (Macdonald & Tonkin, 2008). Invasive species can be introduced into a new region through three broad mechanisms: the importation of a product, the arrival of a transport vector or natural spread from a neighbouring region where the alien species is already established (Mendoza et al., 2014).
Within molluscs, many species have been considered as invasive in freshwater ecosystems (Karatayev et al., 2009). They are represented mainly by Bivalvia, such as the Asian clam Corbicula fluminea (O.F. Müller, 1774) (Domagała et al., 2004), and the zebra mussel Dreissena polymorpha (Pallas, 1771) (Reeders & de Vaate 1990), but also by Gastropoda, such as the apple snail Pomacea canaliculata (Lamarck, 1828) (Estebenet & Martín, 2002). Another good example of biological invasion success in phylum Gastropoda is the New Zealand mudsnail Potamopyrgus antipodarum (J.E. Gray, 1843), which is one of the most successful invasive freshwater mollusc species worldwide. It has invaded a wide variety of freshwater and estuarine habitats in all continents, except for Antarctica and Africa (Collado, 2014; Alonso et al., 2019; Levri et al., 2020).
In this paper, we report the first finding of established populations of the New Zealand mudsnail Potamopyrgus antipodarum in the African continent, in Morocco. We discuss possible mechanisms of introduction. Moreover, we aim to increase awareness on the impacts of invasive species on native fauna in Morocco.
Material and methodsTop
STUDY AREA
The Moulouya River, with its length of almost 600 km, is one of the longest rivers of Morocco and the Maghreb. It is located in the northeast of the country and flows into the Mediterranean Sea. Its main permanent tributaries are the Ansegmir, Melloulou, Za and Msoun rivers. Other tributaries are currently intermittent (three to five flash floods on average per year) (Mabrouki et al., 2019b; Taybi et al., 2020a). The Site of Biological and Ecological Interest (SIBE) of the lower Moulouya extends over an area of almost 3000 ha, over a length of 25 km (Fig. 1). It presents various aquatic ecosystems, including the mouth of the Moulouya River and its floodplain, the coastal marine strip 6 km in length, the dune ridge, salt marshes with semi-temporary immersion and a river channel of 7 km length (Dakki et al., 2003).
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Fig. 1.— Ubicación del sitio Ramsar del humedal Moulouya, el área de distribución y el tipo de hábitat (manantial Chrarba) de Potamopyrgus antipodarum (J.E. Gray, 1843) en Marruecos. |
SAMPLING
During field surveys conducted from 2014 to 2020, more than 100 localities were investigated in Eastern Morocco and the Moulouya River basin (see Mabrouki et al., 2020a for additional details on localities). Most of these sampling sites were visited at least three times. The samples of benthic fauna including molluscs were collected with a Surber sampler (surface of 20 × 25 cm and 0.4 mm mesh net). Conductivity, pH, dissolved oxygen and temperature were measured in situ with a multiparametric measuring device (WTW, MultiLine P4).
The measurements of the shells were carried out using a stereo microscope (ZEISS); the photographs were taken with a digital camera system (Leica R8). The map was made using ArcGIS software.
ResultsTop
New Zealand mudsnails were detected in three locations of the >100 water bodies prospected (Fig. 1, Table 1), most of them brackish or moderately mineralized, near to the coast and always at low altitude. About 400 individuals have been collected (Fig. 2). We dissected eight specimens (all females). The habitats range between the spring of Chrarba, the potamal section of the Moulouya River and the artificial canal of Saidia; all these localities belong to the Ramsar site of the low Moulouya wetland. Our observations represent the first records of established populations of P. antipodarum in Morocco and in the African continent.
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Fig. 2.— Hábitus de Potamopyrgus antipodarum (J.E. Gray, 1843). |
| Locality | Dates | GPS coordinates | Abundance per m2 | Habitat | pH | Temperature °C | Conductivity µs/cm | Dissolved oxygen mg/l | Depth cm | Water speed cm.s–1 | Type of substrat |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Chrarba | 30/07/18 | 35°06’18.7”N 2°20’45.0”W |
250 | spring | 7.5 | 25 | 2030 | 8 | 50 | 25 | mud |
| Pont Moulouya | 16/06/19 | 35°06’32.6”N 2°21’41.9”W |
20 | River | 7.2 | 26 | 4700 | 7.5 | 80 | 5 | mud |
| Canal Saidia | 16/06/19 | 35°06’20.6”N 2°20’42.4”W |
140 | Artificial canal | 7.8 | 25 | 1950 | 7 | 40 | 25 | mud |
DiscussionTop
The New Zealand mudsnail has successfully spread through fast rivers, slow-flowing and fresh, brackish and saline water ecosystems all around the world, including lakes, streams, and estuaries (Naser & Son, 2009). In some invaded areas, the densities of the species can exceed 500 000 m2 (Hall et al., 2006). The number of individuals of P. antipodarum collected was relatively low in this first study. This suggests the invasion could be in its initial stage. It is expected that the species range will increase exponentially across the five continents. In European waters the species has been present for more than 100 years, and its further expansion in temperate freshwater ecosystems is still ongoing (Rakauskas et al., 2007; Butkus et al., 2014), which is already noted in the neighbouring invaded areas. Alonso et al. (2019) have shown that the species has invaded the entire Iberian Peninsula and it is in a clear spreading phase, which makes its control very difficult, especially because of its non-water mediated dispersion mechanisms (e.g., mud or birds). This is the reason why it has been recently added to the top “hundred worst” alien species and the third “worst alien” mollusc (Nentwig et al., 2018).
Several hypotheses regarding the introduction of P. antipodarum have been proposed; some of them suggest shipping, either in ballast waters or water tanks. Long/short distance transport means related to commercial movements of aquarium and ornamental fish and plant trade have been also reported. In addition to transport on mud, fishing tools or recreational vessels, the mud snails may also travel by hitchhiking on bird legs or even inside the gut of birds or fishes (Zaranko et al., 1997; Alonso & Castro-Díez, 2008; DFO, 2011). Waterfowl may be the main vectors for inland spread in Northern Africa, since many routes of bird migration between Europe and Africa cross the Iberian Peninsula and Morocco (Pérez-Tris & Santos, 2004; Alonso et al., 2019).
The enormous worldwide invasion success of the species is attributed to several biological features, including opportunistic diet, high growth rates, high ability to escape from predators and other related behavioural traits, parthenogenetic reproduction, and high degree of tolerance to desiccation and a wide range of abiotic parameters (Koetsier, 2006; Rakauskas et al., 2007; Adema et al., 2009; Drown et al., 2011; Levri et al., 2020).
Alien and invasive species keep being recorded from the aquatic ecosystems of Morocco, leading to the formation of new communities of species with diverse interactions and unpredictable damages, especially in freshwater ecosystems including the Moulouya River basin (Mabrouki et al., 2020b; Taybi & Mabrouki 2020; Taybi et al., 2020b, 2020c). This unique ecosystem is home for a diverse array of animal and plant species, many of which are endemic, rare and vulnerable, including freshwater molluscs such as Aghbalia aghbalensis Glöer, Mabrouki & Taybi, 2020, Islamia tifertiensis Glöer, Mabrouki & Taybi, 2020; Theodoxus numidicus (Récluz, 1841) and Unio foucauldianus Pallary, 1936 (Taybi et al., 2017; Glöer et al., 2020; Mabrouki et al., 2020c). In addition to habitat destruction and deterioration of the quality of surface waters currently occurring in Morocco (Mabrouki et al., 2017; Taybi et al., 2020d), global change may increase the chance of success of exotic species by reducing the fitness of local species in the new environment (Dukes & Mooney, 1999). Many of the Moroccan endemic species would see their regional distribution greatly reduced or may even disappear. Given the absence of rigorous international databases that track species in real time and huge research gaps for invasive species in Morocco, in particular, or in Africa in general, a comprehensive and thorough knowledge of the current invasive species distribution at country or continental scale is necessary to ensure their effective management.